Assembly of the Type II Secretion System Such As Found in Vibrio Cholerae Depends on the Novel Pilotin AspS

Overview

Journal PLoS Pathog

Specialty Microbiology

Date 2013 Jan 18

PMID 23326233

Citations 32

Authors

Rhys A Dunstan

Eva Heinz

Lakshmi C Wijeyewickrema

Robert N Pike

Anthony W Purcell

Timothy J Evans

Judyta Praszkier

Roy M Robins-Browne

Richard A Strugnell

Konstantin V Korotkov

Trevor Lithgow

Affiliations

Soon will be listed here.

Abstract

The Type II Secretion System (T2SS) is a molecular machine that drives the secretion of fully-folded protein substrates across the bacterial outer membrane. A key element in the machinery is the secretin: an integral, multimeric outer membrane protein that forms the secretion pore. We show that three distinct forms of T2SSs can be distinguished based on the sequence characteristics of their secretin pores. Detailed comparative analysis of two of these, the Klebsiella-type and Vibrio-type, showed them to be further distinguished by the pilotin that mediates their transport and assembly into the outer membrane. We have determined the crystal structure of the novel pilotin AspS from Vibrio cholerae, demonstrating convergent evolution wherein AspS is functionally equivalent and yet structurally unrelated to the pilotins found in Klebsiella and other bacteria. AspS binds to a specific targeting sequence in the Vibrio-type secretins, enhances the kinetics of secretin assembly, and homologs of AspS are found in all species of Vibrio as well those few strains of Escherichia and Shigella that have acquired a Vibrio-type T2SS.

Citing Articles

Arginine catabolism is essential to polymyxin dependence in Acinetobacter baumannii.

Han M, Alsaadi Y, Zhao J, Zhu Y, Lu J, Jiang X Cell Rep. 2024; 43(7):114410.

PMID: 38923457 PMC: 11338987. DOI: 10.1016/j.celrep.2024.114410.

Defining Membrane Protein Localization by Isopycnic Density Gradients.

Dunstan R, Hay I, Lithgow T Methods Mol Biol. 2023; 2715:91-98.

PMID: 37930523 DOI: 10.1007/978-1-0716-3445-5_6.

Insights into dynamics and gating properties of T2SS secretins.

Barbat B, Douzi B, Ball G, Tribout M, El Karkouri K, Kellenberger C Sci Adv. 2023; 9(40):eadg6996.

PMID: 37792935 PMC: 10550240. DOI: 10.1126/sciadv.adg6996.

Membrane translocation process revealed by in situ structures of type II secretion system secretins.

Yu Z, Wu Y, Chen M, Huo T, Zheng W, Ludtke S Nat Commun. 2023; 14(1):4025.

PMID: 37419909 PMC: 10329019. DOI: 10.1038/s41467-023-39583-2.

Scaffolding Protein GspB/OutB Facilitates Assembly of the Dickeya dadantii Type 2 Secretion System by Anchoring the Outer Membrane Secretin Pore to the Inner Membrane and to the Peptidoglycan Cell Wall.

Zhang S, Gu S, Rycroft P, Ruaudel F, Delolme F, Robert X mBio. 2022; 13(3):e0025322.

PMID: 35546537 PMC: 9239104. DOI: 10.1128/mbio.00253-22.

References

Murshudov G, Skubak P, Lebedev A, Pannu N, Steiner R, Nicholls R . REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr. 2011; 67(Pt 4):355-67. PMC: 3069751. DOI: 10.1107/S0907444911001314. View

Cianciotto N . Type II secretion: a protein secretion system for all seasons. Trends Microbiol. 2005; 13(12):581-8. DOI: 10.1016/j.tim.2005.09.005. View

Finn R, Clements J, Eddy S . HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 2011; 39(Web Server issue):W29-37. PMC: 3125773. DOI: 10.1093/nar/gkr367. View

Coulthurst S, Palmer T . A new way out: protein localization on the bacterial cell surface via Tat and a novel Type II secretion system. Mol Microbiol. 2008; 69(6):1331-5. DOI: 10.1111/j.1365-2958.2008.06367.x. View

Hardie K, Lory S, Pugsley A . Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J. 1996; 15(5):978-88. PMC: 449992. View

Datsenko K, Wanner B . One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A. 2000; 97(12):6640-5. PMC: 18686. DOI: 10.1073/pnas.120163297. View

Bos M, Robert V, Tommassen J . Biogenesis of the gram-negative bacterial outer membrane. Annu Rev Microbiol. 2007; 61:191-214. DOI: 10.1146/annurev.micro.61.080706.093245. View

Guilvout I, Chami M, Berrier C, Ghazi A, Engel A, Pugsley A . In vitro multimerization and membrane insertion of bacterial outer membrane secretin PulD. J Mol Biol. 2008; 382(1):13-23. DOI: 10.1016/j.jmb.2008.06.055. View

Webb C, Selkrig J, Perry A, Noinaj N, Buchanan S, Lithgow T . Dynamic association of BAM complex modules includes surface exposure of the lipoprotein BamC. J Mol Biol. 2012; 422(4):545-55. PMC: 3433275. DOI: 10.1016/j.jmb.2012.05.035. View

10.

Johnson T, Abendroth J, Hol W, Sandkvist M . Type II secretion: from structure to function. FEMS Microbiol Lett. 2006; 255(2):175-86. DOI: 10.1111/j.1574-6968.2006.00102.x. View

11.

Krissinel E, Henrick K . Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr. 2004; 60(Pt 12 Pt 1):2256-68. DOI: 10.1107/S0907444904026460. View

12.

Castresana J . Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000; 17(4):540-52. DOI: 10.1093/oxfordjournals.molbev.a026334. View

13.

Holm L, Rosenstrom P . Dali server: conservation mapping in 3D. Nucleic Acids Res. 2010; 38(Web Server issue):W545-9. PMC: 2896194. DOI: 10.1093/nar/gkq366. View

14.

Crivat G, Taraska J . Imaging proteins inside cells with fluorescent tags. Trends Biotechnol. 2011; 30(1):8-16. PMC: 3246539. DOI: 10.1016/j.tibtech.2011.08.002. View

15.

Thanassi D, Hultgren S . Multiple pathways allow protein secretion across the bacterial outer membrane. Curr Opin Cell Biol. 2000; 12(4):420-30. DOI: 10.1016/s0955-0674(00)00111-3. View

16.

Lesley S, Wilson I . Protein production and crystallization at the joint center for structural genomics. J Struct Funct Genomics. 2005; 6(2-3):71-9. DOI: 10.1007/s10969-005-2897-2. View

17.

Collin S, Guilvout I, Nickerson N, Pugsley A . Sorting of an integral outer membrane protein via the lipoprotein-specific Lol pathway and a dedicated lipoprotein pilotin. Mol Microbiol. 2011; 80(3):655-65. DOI: 10.1111/j.1365-2958.2011.07596.x. View

18.

Parsot C, Taxman E, Mekalanos J . ToxR regulates the production of lipoproteins and the expression of serum resistance in Vibrio cholerae. Proc Natl Acad Sci U S A. 1991; 88(5):1641-5. PMC: 51080. DOI: 10.1073/pnas.88.5.1641. View

19.

Frickey T, Lupas A . CLANS: a Java application for visualizing protein families based on pairwise similarity. Bioinformatics. 2004; 20(18):3702-4. DOI: 10.1093/bioinformatics/bth444. View

20.

Bouley J, Condemine G, Shevchik V . The PDZ domain of OutC and the N-terminal region of OutD determine the secretion specificity of the type II out pathway of Erwinia chrysanthemi. J Mol Biol. 2001; 308(2):205-19. DOI: 10.1006/jmbi.2001.4594. View